Eradication of intracellular Francisella tularensis in THP-1 human macrophages with a novel autophagy inducing agent

Journal of Biomedical Science

Volumn 16, Issue , 2009, Pages

  Chiu, Hao Chieh ^a   Soni, Shilpa ^a   Kulp, Samuel K ^a   Curry, Heather ^a   Wang, Dasheng ^a   Gunn, John S ^a,b   Schlesinger, Larry S ^a,b   Chen, Chingshih ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Celecoxib; Chloroquine; Intracellular Bacterium; Intracellular Survival; Unfold Protein Response

Indexed keywords

2 AMINO N [4 [5 (2 PHENANTHRENYL) 3 TRIFLUOROMETHYL 1H PYRAZOL 1 YL]PHENYL]ACETAMIDE; ANTIINFECTIVE AGENT; BACTERIAL VACCINE; CHLOROQUINE; ENZYME INHIBITOR; PYRAZOLE DERIVATIVE; SULFONAMIDE;

ARTICLE; AUTOPHAGY; CELL LINE; CHEMISTRY; FLUORESCENCE MICROSCOPY; FRANCISELLA TULARENSIS; HUMAN; IMMUNOLOGY; LYSOSOME; MACROPHAGE; METABOLISM; METHODOLOGY; MICROBIOLOGY; TIME; TULAREMIA;

ANTI-INFECTIVE AGENTS; AUTOPHAGY; BACTERIAL VACCINES; CELL LINE; CHLOROQUINE; ENZYME INHIBITORS; FRANCISELLA TULARENSIS; HUMANS; LYSOSOMES; MACROPHAGES; MICROSCOPY, FLUORESCENCE; PYRAZOLES; SULFONAMIDES; TIME FACTORS; TULAREMIA;

EID: 76249102863     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1186/1423-0127-16-110     Document Type: Article

References (42)

1. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y: Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009, 10:458-467.
2. Orvedahl A, Levine B: Eating the enemy within: autophagy in infectious diseases. Cell Death Differ 2009, 16:57-69.
3. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V: Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004, 119:753-766.
4. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, Nara A, Funao J, Nakata M, Tsuda K, Hamada S, Yoshimori T: Autophagy defends cells against invading group A Streptococcus. Science 2004, 306:1037-1040.
5. Birmingham CL, Smith AC, Bakowski MA, Yoshimori T, Brumell JH: Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem 2006, 281:11374-11383.
6. Ellis J, Oyston PC, Green M, Titball RW: Tularemia. Clin Microbiol Rev 2002, 15:631-646.
7. Oyston PC: Francisella tularensis: unravelling the secrets of an intracellular pathogen. J Med Microbiol 2008, 57:921-930.
8. Sjostedt A: Virulence determinants and protective antigens of Francisella tularensis. Curr Opin Microbiol 2003, 6:66-71.
9. Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Friedlander AM, Hauer J, Layton M, Lillibridge SR, McDade JE, Osterholm MT, O'Toole T, Parker G, Perl TM, Russell PK, Tonat K: Tularemia as a biological weapon: medical and public health management. Jama 2001, 285:2763-2773.
10. Oyston PC, Sjostedt A, Titball RW: Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat Rev Microbiol 2004, 2:967-978.
11. Alibek K: Biohazard New York, NY: Random House; 1999.
12. Clemens DL, Lee BY, Horwitz MA: Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infect Immun 2004, 72:3204-3217.
13. Santic M, Asare R, Skrobonja I, Jones S, Abu Kwaik Y: Acquisition of the vacuolar ATPase proton pump and phagosome acidification are essential for escape of Francisella tularensis into the macrophage cytosol. Infect Immun 2008, 76:2671-2677.
14. Mohapatra NP, Balagopal A, Soni S, Schlesinger LS, Gunn JS: AcpA is a Francisella acid phosphatase that affects intramacrophage survival and virulence. Infect Immun 2007, 75:390-396.
15. Mariathasan S, Weiss DS, Dixit VM, Monack DM: Innate immunity against Francisella tularensis is dependent on the ASC/cas-pase-1 axis. J Exp Med 2005, 202:1043-1049.
16. Lai XH, Golovliov I, Sjostedt A: Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infect Immun 2001, 69:4691-4694.
17. Checroun C, Wehrly TD, Fischer ER, Hayes SF, Celli J: Autophagymediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc Natl Acad Sci USA 2006, 103:14578-14583.
18. Mohapatra NP, Soni S, Reilly TJ, Liu J, Klose KE, Gunn JS: Combined deletion of four Francisella novicida acid phosphatases attenuates virulence and macrophage vacuolar escape. Infect Immun 2008, 76:3690-3699.
19. Santic M, Akimana C, Asare R, Kouokam JC, Atay S, Kwaik YA: Intracellular fate of Francisella tularensis within arthropodderived cells. Environ Microbiol 2009, 11(6):1473-81.
20. Zhu J, Huang J-W, Tseng P-H, Yang Y-T, Fowble J, Shiau C-W, Shaw Y-J, Kulp SK, Chen C-S: From the Cyclooxygenase-2 Inhibitor Celecoxib to a Novel Class of 3-Phosphoinositide-Dependent Protein Kinase-1 Inhibitors. Cancer Res 2004, 64:4309-4318.
21. Balagopal A, MacFarlane AS, Mohapatra N, Soni S, Gunn JS, Schlesinger LS: Characterization of the receptor-ligand pathways important for entry and survival of Francisella tularensis in human macrophages. Infect Immun 2006, 74:5114-5125.
22. Gavrilin MA, Bouakl IJ, Knatz NL, Duncan MD, Hall MW, Gunn JS, Wewers MD: Internalization and phagosome escape required for Francisella to induce human monocyte IL-1beta processing and release. Proc Natl Acad Sci USA 2006, 103:141-146.
23. Jeffrey M, Edmondson LSAaAOM: A rapid and simple MTT-based spectrophotometric assay for determining drug sensitivity in monolayer cultures. Methods in Cell Science 1988, 11(1):3.
24. Racher AJ, Looby D, Griffiths JB: Use of lactate dehydrogenase release to assess changes in culture viability. Cytotechnology 1990, 3:301-307.
25. Park MA, Curiel DT, Koumenis C, Graf M, Chen CS, Fisher PB, Grant S, Dent P: PERK-dependent regulation of HSP70 expression and the regulation of autophagy. Autophagy 2008, 4:364-367.
26. Park M, Yacoub A, Rahmani M, Zhang G, Hart L, Hagan M, Calderwood S, Sherman M, Koumenis C, Spiegel S, Chen CS, Graf M, Curiel D, Fisher P, Grant S, Dent P: OSU-03012 stimulates PERKdependent increases in HSP70 expression, attenuating its lethal actions in transformed cells. Mol Pharmacol 2008, 73:1168-1184.
27. Gao M, Yeh PY, Lu YS, Hsu CH, Chen KF, Lee WC, Feng WC, Chen CS, Kuo ML, Cheng AL: OSU-03012 a novel celecoxib derivative, induces reactive oxygen species-related autophagy in hepatocellular carcinoma. Cancer Res 3012, 68:9348-9357.
28. Chiu HC, Kulp SK, Soni S, Wang D, Gunn JS, Schlesinger LS, Chen CS: Eradication of intracellular Salmonella enterica serovar Typhimurium with a small-molecule, host cell-directed agent. Antimicrob Agents Chemother 2009, 53:5236-5244.
29. Finlay BB, Hancock RE: Can innate immunity be enhanced to treat microbial infections? Nat Rev Microbiol 2004, 2:497-504.
30. Weng SC, Kashida Y, Kulp SK, Wang D, Brueggemeier RW, Shapiro CL, Chen CS: Sensitizing estrogen receptor-negative breast cancer cells to tamoxifen with OSU-03012 a novel celecoxibderived phosphoinositide-dependent protein kinase-1/Akt signaling inhibitor. Mol Cancer Ther 3012, 7:800-808.
31. Wang YC, Kulp SK, Wang D, Yang CC, Sargeant AM, Hung JH, Kashida Y, Yamaguchi M, Chang GD, Chen CS: Targeting endoplasmic reticulum stress and Akt with OSU-03012 and gefitinib or erlotinib to overcome resistance to epidermal growth factor receptor inhibitors. Cancer Res 2008, 68:2820-2830.
32. Cullinane M, Gong L, Li X, Lazar-Adler N, Tra T, Wolvetang E, Prescott M, Boyce JD, Devenish RJ, Adler B: Stimulation of autophagy suppresses the intracellular survival of Burkholderia pseudomallei in mammalian cell lines. Autophagy 2008, 4:744-753.
33. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C: Escape of Intracellular Shigella from Autophagy. Science 2005, 307:727-731.
34. Amer AO, Swanson MS: Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol 2005, 7:765-778.
35. Butchar JP, Cremer TJ, Clay CD, Gavrilin MA, Wewers MD, Marsh CB, Schlesinger LS, Tridandapani S: Microarray analysis of human monocytes infected with Francisella tularensis identifies new targets of host response subversion. PLoS ONE 2008, 3:e2924.
36. Cremer TJ, Amer A, Tridandapani S, Butchar JP: Francisella tularensis regulates autophagy-related host cell signaling pathways. Autophagy 2009, 5:125-128.
37. Zhu J, Huang JW, Tseng PH, Yang YT, Fowble J, Shiau CW, Shaw YJ, Kulp SK, Chen CS: From the cyclooxygenase-2 inhibitor celecoxib to a novel class of 3-phosphoinositide-dependent protein kinase-1 inhibitors. Cancer Res 2004, 64:4309-4318.
38. Porchia LM, Guerra M, Wang YC, Zhang Y, Espinosa AV, Shinohara M, Kulp SK, Kirschner LS, Saji M, Chen CS, Ringel MD: 2-amino-N-{4-[5-(2-phenanthrenyl)-3-(trifluoromethyl)-1H-pyrazol-1-yl]-phe nyl} acetamide (OSU-03012), a celecoxib derivative, directly targets p21-activated kinase. Mol Pharmacol 2007, 72:1124-1131.
39. Yacoub A, Park MA, Hanna D, Hong Y, Mitchell C, Pandya AP, Harada H, Powis G, Chen CS, Koumenis C, Grant S, Dent P: OSU-03012 promotes caspase-independent but PERK-, cathepsin B-, BID-, and AIF-dependent killing of transformed cells. Mol Pharmacol 2006, 70:589-603.
40. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback JA, Urano F, Imaizumi K: Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006, 26:9220-9231.
41. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E, Momoi T: ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007, 14:230-239.
42. Schonthal AH: Direct non-cyclooxygenase-2 targets of celecoxib and their potential relevance for cancer therapy. Br J Cancer 2007, 97:1465-1468.